Synaptic organization of expansion motoneurons of Navanax inermis

Abstract

The opisthobranch mollusc, Navanax, feeds by rapid pharyngeal expansion that sucks in prey followed by peristaltic swallowing that moves prey into the esophagus. Several identifiable neurons on the ventral surface of the buccal ganglia control radial musculature within the pharyngeal wall, contraction of which leads to pharyngeal expansion. These are considered expansion motoneurons because their axons run into the muscle and twitches and EMGs occur one for one with action potentials. The motoneurons are electrotonically coupled. Electrotonic PSPs, the components of spread associated with impulses, can summate with subthreshold DC depolarizations to yield synchronous impulses in coupled cells. During a train of responses the later electrotonic PSPs can be facilitated because of increase in amplitude and duration of the presynaptic impulses. Expansion motoneurons are synaptically connected by two apparently interneuronal pathways: a low threshold pathway activated by subthreshold depolarization of the two largest expansion motoneurons (the G-cells) that inhibits the entire population, and a high threshold pathway that is activated by a train of G-cell impulses and produces largely excitatory PSPs in the smaller expansion motoneurons and an EPSP--IPSP sequence in the G-cells. Coupling among expansion motoneurons can be abolished by chemical inhibitory synaptic inputs that are activated by electrical stimulation of the pharyngeal nerve or tactile stimulation of the pharyngeal wall. This uncoupling phenomenon can be explained by a simple equivalent circuit in which inhibitory synapses along the coupling pathway short circuit electrotonic spread. Uncoupling can outlast the evoking stimulus by several seconds. During uncoupling the smaller expansion motoneurones can fire independently while the G-cell is inhibited, and impulses still propagate from somata to the periphery. The expansion motoneuron population receives excitatory input from the mechanoreceptors in protractor muscles. Mechanical stimulation of the pharyngeal wall activates primary sensory neurons in the buccal ganglia that fire during excitation and during inhibition and uncoupling of expansion motoneurons.